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Diffusion tensor imaging in human subjects wearing metallic orthodontic braces
Xinyuan Miao1,2, Yuankui Wu1,2,3, Dapeng Liu1,2, Hangyi Jiang1, Qin Qin1,2, Peter C.M van Zijl1,2, Jay J. Pillai4,5, and Jun Hua1,2
1Neurosection, Division of MRI Research, Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, MD, United States, 2F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, United States, 3Department of Medical Imaging, Nanfang Hospital, Southern Medical University, Guangzhou, China, 4Johns Hopkins University School of Medicine, Division of Neuroradiology, Russell H. Morgan Department of Radiology and Radiological Science, Baltimore, MD, United States, 5Department of Neurosurgery, Johns Hopkins University School of Medicine, Baltimore, MD, United States

Synopsis

Metallic objects such as dental braces bring substantial susceptibility artifacts in MR images acquired using echo-planar-imaging (EPI) sequences. Here, we demonstrate that diffusion-prepared diffusion tensor imaging (DTI) with three-dimensional fast gradient-echo readout can significantly reduce susceptibility artifacts that are commonly seen in conventional spin-echo (SE) EPI DTI in the presence of metallic orthodontic braces.

Introduction

Dental fillings and orthodontic braces containing various metals can cause large susceptibility artifacts extending from the facial region into the brain1,2,3 in commonly used echo-planar imaging (EPI) based sequences. This is particularly a problem for diffusion-tensor-imaging (DTI) MRI studies4, where spin echo (SE)-EPI sequences are commonly used. Such susceptibility artifacts include signal dropout and geometric distortion in affected regions. SE-EPI in principle has less signal dropouts than gradient echo (GRE) EPI. However, geometric distortion due to local B0 inhomogeneity can still be significant in SE-EPI. Therefore, many DTI studies choose to acquire two identical DTI scans with opposite phase encoding directions in order to correct for such distortion, at the expense of doubling scan time and introducing potential motion and physiological variations between scans5. Alternatively, diffusion contrasts can be induced using spin preparation modules before readout6,7 which separates contrast generation from the readout, thereby opening the possibility to use virtually any pulse sequence for image acquisition. Among the various strategies, a double refocusing diffusion preparation module followed by a 3D readout has been commonly adopted8,9, which can significantly reduce image distortion commonly seen in EPI10. In this study, we applied a diffusion-prepared-DTI approach8,11 with single-shot 3D fast-gradient-echo (GRE) readout in healthy human subjects wearing metallic orthodontic braces to evaluate its ability to minimize susceptibility artifacts in the presence of metallic objects12.

Methods

Six healthy participants (40±6yo, 3 females) were recruited for this study. Removable dental braces with bonding trays were used so that MRI images can be acquired with braces or without braces in the same participants. Figure 1 illustrates the DTI sequences. The diffusion-prepared DTI sequence includes a diffusion preparation module for generating the desired diffusion contrast, followed by a single-shot 3D fast GRE readout. The diffusion preparation module uses double refocusing pulses, with additional diffusion weighting gradients inserted between the RF pulses6,7,13,14. To minimize eddy current related artifacts and reduce T1 effects during the readout, a stimulated echo scheme8 is adopted: a dephasing gradient in the slice-encoding direction before the last 90° pulse in the diffusion preparation module, and a set of rephasing gradients in the readout (each of which has the same area as the dephasing gradient) are added. The following scans were acquired for each subject on a 3T Philips MRI scanner: MPRAGE (voxel=1x1x1mm3); SE-EPI DTI: b=0 and 800s/mm2, 15 diffusion gradient directions voxel=2.5x2.5x2.5mm3; diffusion-prepared DTI: same b-values, diffusion gradients and voxel size as SE-EPI DTI, TR/TE(effective)=5000/90ms, FA=11°, SENSE factor=3x1, centric order, TRGRE/TEGRE=4.1/2.1ms, dephasing gradient=2mT/m and 5ms. DTI data were processed using MRI-Studio (www.mristudio.org). Signal-to-noise-ratio (SNR), apparent-diffusion-coefficient (ADC) and fractional-anisotropy (FA) were compared in two manually drawn ROIs: bilateral inferior fronto-occipital fasciculus (IFOF) with strong susceptibility artifacts, and bilateral posterior limb of internal capsule (PLIC) with minimal susceptibility artifacts in EPI. Geometric distortion was visualized using Slicer in FSL (https://fsl.fmrib.ox.ac.uk/), and quantified by the Jaccard index, which ranges from zero to one, indicating no overlap to complete agreement, respectively, between the geometric shapes of the DTI image and reference structural images.

Results

Figure 2 shows typical raw diffusion-weighted images, ADC, and color-coded FA maps from one subject wearing braces. While SE-EPI shows signal loss in many brain regions (e.g. the frontal lobe in the slice shown), no obvious artifacts were visible in the diffusion-prepared EPI in the entire brain. Color coded FA maps obtained from SE-EPI DTI showed spurious results in the inferior frontal lobe near the brace (red arrow in Figure 2), affecting visualization of the IFOF, as compared to diffusion-prepared color FA maps in the same subject. Geometric distortion (Figure 3) was minimal in diffusion-prepared DTI, but was substantial in SE-EPI DTI (significantly lower Jaccard index in each slice, P < .001), and the degree of distortion varied with the location of the slice. Table 1 summarizes the group-averaged quantitative results from all subjects from the ROI analysis (ROIs delineated in Figure 2). ADC, FA and SNR values were all comparable between diffusion-prepared and SE-EPI in the PLIC, a structure minimally affected by the susceptibility artifacts. In the IFOF, which is close to the dental braces, SNR was significantly diminished in SE-EPI, leading to erroneous ADC and FA values, whereas diffusion-prepared DTI showed greater SNR and reasonable ADC and FA values consistent with the literature16. When the same scans were repeated in the same subjects without wearing the metallic dental braces, ADC, FA and SNR in both the PLIC and the IFOF became comparable between SE-EPI and diffusion-prepared DTI scans, all of which are within the typical range reported in the literature.

Discussion & Conclusion

We demonstrate that diffusion-prepared-DTI can acquire diffusion MR images in healthy human subjects wearing metallic dental braces with preserved SNR for the entire brain, whereas conventional SE-EPI DTI showed significantly reduced SNR in regions with strong susceptibility effects. Also, the geometric distortion was reduced significantly with diffusion-prepared DTI. This technique is expected to provide an alternative approach in studies involving regions with large susceptibility artifacts caused by metallic implants in the brain.

Acknowledgements

NINDS (1R01NS108452), NIBIB (R21EB 023538 and P41 EB015909), NICHD (U54 HD079123).

References

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5. Sotiropoulos SN, Jbabdi S, Xu J, et al. Advances in diffusion MRI acquisition and processing in the Human Connectome Project. Neuroimage. 2013;80:125-143. doi:10.1016/J.NEUROIMAGE.2013.05.057 6. Lee H, Price RR. Diffusion imaging with the MP-rage sequence. J Magn Reson Imaging. 1994;4(6):837-842. doi:10.1002/jmri.1880040616

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12. Miao X, Wu Y, Liu D, et al. Whole-brain functional and diffusion tensor mri in human participants with metallic orthodontic braces. Radiology. (in press)

13. Coremans J, Spanoghe M, Budinsky L, et al. A Comparison between Different Imaging Strategies for Diffusion Measurements with the Centric Phase-Encoded TurboFLASH Sequence. J Magn Reson. 1997;124(2):323-342. doi:10.1006/JMRE.1996.1025

14. Thomas DL, Pell GS, Lythgoe MF, Gadian DG, Ordidge RJ. A quantitative method for fast diffusion imaging using magnetization-prepared turboFLASH. Magn Reson Med. 1998;39(6):950-960. doi:10.1002/mrm.1910390613

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Figures

Figure 1: Pulse sequence diagrams of, A: 3D diffusion-prepared diffusion tensor imaging (DTI) (To minimize eddy current–related artifacts and to reduce T1 effects during readout, a stimulated-echo scheme8,15 was adopted in diffusion-prepared DTI), and, B: conventional 2D multislice spin-echo (SE) EPI DTI. One entire image volume was acquired in a single repetition time (TR) period in all sequences to avoid the well-known phase errors in multishot approaches.

Figure 2. SE-EPI and diffusion-prepared DTI axial images acquired at 3.0 T in a participant wearing metallic dental braces. A, raw diffusion-weighted images, B, calculated ADC maps, and, C, fractional anisotropy map color coded by V1 orientation (standard red, green, and blue convention). Susceptibility artifacts were observed on SE EPI images in regions close to brace (arrow). No obvious artifacts were seen on diffusion-prepared DTI image. Regions of interest of IFOF and PLIC used in subsequent quantitative analysis are highlighted on diffusion-prepared DTI images with red.

Figure 3. Geometric distortions in axial SE-EPI (top row) and diffusion-prepared (bottom row) DTI when compared with MPRAGE images in same participant wearing metallic dental braces. Edges of brain structures obtained from coregistered MPRAGE images are shown in red contour lines on mean diffusion-weighted images from the two DTI approaches. Mismatch between contour lines and edge of structures shown in DTI images illustrates geometric distortion artifacts (eg, frontal area indicated by arrow). Mean Jaccard index (JI) is calculated for each slice and is listed under each image.

Table 1. Group-averaged quantitative results from all subjects (n=6) for the comparison of the SE-EPI and diffusion-prepared DTI approaches. In the IFOF close to the braces, SNR was significantly diminished in SE-EPI-DTI, whereas diffusion-prepared-DTI showed greater SNR, ADC and FA.

Proc. Intl. Soc. Mag. Reson. Med. 28 (2020)
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